Neural control of vergence eye movements: neurons encoding vergence velocity.

Single-unit recordings were made from midbrain areas in monkeys trained to make both conjugate and disjunctive (vergence) eye movements. Previous work had identified cells with a firing rate proportional to the vergence angle, without regard to the direction of conjugate gaze. The present study describes the activity of neurons that burst for disjunctive eye movements. Convergence burst cells display a discrete burst of activity just before and during convergence eye movements. For most of these cells, the profile of the burst is correlated with instantaneous vergence velocity and the number of spikes in the burst is correlated with the size of the vergence movement. Some of these cells also have a tonic firing rate that is positively correlated with vergence angle (convergence burst-tonic cells). Divergence burst cells have similar properties, except that they fire for divergent and not convergent movements. Divergence burst cells are encountered far less often than convergence burst cells. Both convergence and divergence burst cells were found in an area of the mesencephalic reticular formation just dorsal and lateral to the oculomotor nucleus. Convergence burst cells were also recorded in another more dorsal mesencephalic region, rostral to the superior colliculus. Both of the areas also contain cells that encode vergence angle. Models of the vergence system derived from psychophysical data imply the existence of a vergence integrator, the output of which is vergence angle. Some models also suggest the presence of a parallel element that improves the frequency response of the vergence system, but has no effect on the steady-state behavior of the system. Vergence burst cells would be suitable inputs to a vergence integrator. By providing a vergence velocity signal to motoneurons, they may improve the dynamic response of the vergence system. The behavior of vergence burst cells during vergence movements is similar to that of the medium-lead burst cells during saccades. The proposed roles for vergence velocity cells are analogous to those of the saccadic burst cells. In this respect, the neural organization of the vergence system resembles that of the saccadic system, despite the distinct difference in the kinematics of these two types of eye movements.

[1]  G. Westheimer,et al.  Disjunctive eye movements , 1961, The Journal of physiology.

[2]  D. Robinson,et al.  Abducens unit behavior in the monkey during vergence movements. , 1972, Vision research.

[3]  J. C. Kotulak,et al.  The dissociability of accommodation from vergence in the dark. , 1986, Investigative ophthalmology & visual science.

[4]  E. Keller Participation of medial pontine reticular formation in eye movement generation in monkey. , 1974, Journal of neurophysiology.

[5]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. , 1971, Journal of neurophysiology.

[6]  L. Mays Neural control of vergence eye movements: convergence and divergence neurons in midbrain. , 1984, Journal of neurophysiology.

[7]  D. Cogan,et al.  Internuclear Ophthalmoplegia: A Review of Fifty-Eight Cases , 1959 .

[8]  E. Keller Accommodative vergence in the alert monkey. Motor unit analysis. , 1973, Vision research.

[9]  Lawrence W. Stark,et al.  Dynamical Characteristics of the Fusional Vergence Eye-Movement System , 1968, IEEE Trans. Syst. Sci. Cybern..

[10]  V. V. Krishnan,et al.  A Heuristic Model for the Human Vergence Eye Movement System , 1977, IEEE Transactions on Biomedical Engineering.

[11]  S. Gielen,et al.  A quantitative analysis of generation of saccadic eye movements by burst neurons. , 1981, Journal of neurophysiology.

[12]  S. Highstein,et al.  Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons , 1986, The Journal of comparative neurology.

[13]  L E Mays,et al.  Neural control of vergence eye movements: activity of abducens and oculomotor neurons. , 1984, Journal of neurophysiology.

[14]  Shiro Usui,et al.  Digital Low-Pass Differentiation for Biological Signal Processing , 1982, IEEE Transactions on Biomedical Engineering.

[15]  A. Fuchs,et al.  Activity of brain stem neurons during eye movements of alert monkeys. , 1972, Journal of neurophysiology.

[16]  D. Robinson Control of eye movements , 1981 .

[17]  A. Fuchs,et al.  Brainstem control of saccadic eye movements. , 1985, Annual review of neuroscience.

[18]  B G Cumming,et al.  Disparity-induced and blur-induced convergence eye movement and accommodation in the monkey. , 1986, Journal of neurophysiology.

[19]  S. Judge,et al.  Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation. , 1986, Journal of neurophysiology.